Diuronotus Aspetos (Paucitubulatina) Yields Insights Into the Evolution of Organs Systems in Gastrotricha

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Diuronotus Aspetos (Paucitubulatina) Yields Insights Into the Evolution of Organs Systems in Gastrotricha Neuromuscular study of early branching Diuronotus aspetos (Paucitubulatina) yields insights into the evolution of organs systems in Gastrotricha Bekkouche, Nicolas Tarik; Worsaae, Katrine Published in: Zoological Letters DOI: 10.1186/s40851-016-0054-3 Publication date: 2016 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Bekkouche, N. T., & Worsaae, K. (2016). Neuromuscular study of early branching Diuronotus aspetos (Paucitubulatina) yields insights into the evolution of organs systems in Gastrotricha. Zoological Letters, 2, [21]. https://doi.org/10.1186/s40851-016-0054-3 Download date: 08. apr.. 2020 Bekkouche and Worsaae Zoological Letters (2016) 2:21 DOI 10.1186/s40851-016-0054-3 RESEARCH ARTICLE Open Access Neuromuscular study of early branching Diuronotus aspetos (Paucitubulatina) yields insights into the evolution of organs systems in Gastrotricha Nicolas Bekkouche and Katrine Worsaae* Abstract Background: Diuronotus is one of the most recently described genera of Paucitubulatina, one of the three major clades in Gastrotricha. Its morphology suggests that Diuronotus is an early branch of Paucitubulatina, making it a key taxon for understanding the evolution of this morphologically understudied group. Here we test its phylogenetic position employing molecular data, and provide detailed descriptions of the muscular, nervous, and ciliary systems of Diuronotus aspetos, using immunohistochemistry and confocal laser scanning microscopy. Results: We confirm the proposed position of D. aspetos within Muselliferidae, and find this family to be the sister group to Xenotrichulidae. The muscular system, revealed by F-actin staining, shows a simple, but unique organization of the trunk musculature with a reduction to three pairs of longitudinal muscles and addition of up to five pairs of dorso- ventral muscles, versus the six longitudinal and two dorso-ventral pairs found in most Paucitubulatina. Using acetylated α-tubulin immunoreactivity, we describe the pharynx in detail, including new nervous structures, two pairs of sensory cilia, and a unique canal system. The central nervous system, as revealed by immunohistochemistry, shows the general pattern of Gastrotricha having a bilobed brain and a pair of ventro-longitudinal nerve cords. However, in addition are found an anterior nerve ring, several anterior longitudinal nerves, and four ventral commissures (pharyngeal, trunk, pre-anal, and terminal). Two pairs of protonephridia are documented, while other Paucitubulatina have one. Moreover, the precise arrangement of multiciliated cells is unraveled, yielding a pattern of possibly systematic importance. Conclusion: Several neural structures of Diuronotus resemble those found in Xenotrichula (Xenotrichulidae) and may constitute new apomorphies of Paucitubulatina, or even Gastrotricha. In order to test these new evolutionary hypotheses, comparable morphological data from other understudied gastrotrich branches and a better resolution of the basal nodes of the gastrotrich phylogeny are warranted. Nonetheless, the present study offers new insights into the evolution of organ systems and systematic importance of so-far neglected characters in Gastrotricha. Keywords: Neurobiology, Nervous system, Musculature, Ciliary structures, Meiofauna, Chaetonotida, Spiralia, Molecular phylogeny Background kinorhynchs (Nematorhyncha [5]) or Gnathostomulida Gastrotricha are small, often sub-millimetre, interstitial (Neotrichozoa [6, 7]). Later, molecular phylogenies placed worms, ubiquitously found in most aquatic environments them within Spiralia with uncertain affinities; within the with a long debated phylogenetic position [1–3]. They debated group Platyzoa, comprising Gastrotricha, Platy- were first considered closely related to various meiofaunal, helminthes and Gnathifera [1, 8, 9]. Recent phylogenomic protostome groups, such as rotifers (Trochelminthes [4]), studies propose a sister group relationship between Platyhelminthes and Gastrotricha [3, 10]. However, the * Correspondence: [email protected] controversy over the phylogenetic position of Gastro- Marine Biological Section, Department of Biology, University of Copenhagen, tricha masks other problems within the group. Indeed, Universitetsparken 4, 2100 Copenhagen Ø, Denmark © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bekkouche and Worsaae Zoological Letters (2016) 2:21 Page 2 of 29 compared to the diversity and omnipresence of these synapomorphy [34]. These recent reports were used to animals, relatively few phylogenetic and detailed mor- infer the plesiomorphic arrangement of the musculature phological studies have been conducted on this group of Gastrotricha as constituted by two ventro-lateral longi- and the evolution of, e.g., nervous system, muscular sys- tudinal muscles surrounded by outer circular muscles, tem and nephridia is unresolved [11–13]. Its diversity and longitudinal splanchnic muscles surrounded by also remains largely unexplored, as exemplified by the helicoidal and intestinal circular muscles [2]. In Paucitubu- recent erection of the family Hummondasyidae (Macro- latina, the longitudinal muscles appear to be more numer- dasyida) in 2014 [14] and the genera Thaidasys in 2015 ous, and the outer circular muscles, if present, are [15] and Bifidochaetus in 2016 [16]. incomplete and consist of dorso-ventral muscles [2]. These Diuronotus [17] is another recently described gastro- dorso-ventral or semi-circular muscles are found in marine trich genus (2005), comprising two described species: chaetonotids [22], but are often missing or highly reduced Diuronotus aspetos Todaro et al. [17] and, Diuronotus in freshwater chaetonotids [11, 22, 33] emphasizing the im- rupperti Todaro et al. [17], and one undescribed species portance of studying the marine Diuronotus in order to re- Diuronotus sp. [18–20], transferred from Halichaetonotus solve their evolution and contribute to the broader [17]. These are all found in marine interstitial environments understanding of muscular evolution within Gastrotricha. of the North Atlantic; D. aspetos from Greenland [17] and To date, only one confocal study on Xenotrichula has Germany [2, 21], D. rupperti from Denmark [17] and Diur- described the nervous system of a member of Paucitubu- onotus sp. from North Carolina, USA [18]. Diuronotus was latina in detail [12], while it has been extensively described placed in Muselliferidae (Paucitubulatina, Chaetonitida) for Multitubulatina (Neodasys) [13] and in several Macro- next to Musellifer [22] with which it shares the presence of dasyida with combined immunohistochemistry and CLSM a ciliated so-called ‘muzzle’ (or snout) and specific ultra- (e.g., [35, 36]), or transmission electron microscopy structural traits of scales and sperm [23]. (TEM) [37]. One of the conclusions of the Xenotrichula Gastrotricha are divided into two main taxa: the sup- study [13] is the low structural variation of the nervous posedly monophyletic Macrodasyida and the possibly system within Gastrotricha, which always comprises a bi- paraphyletic Chaetonotida, divided further into the Mul- lobed brain with a ventral commissure, a pair of anteriorly titubulatina, (consisting of one genus, Neodasys, and projecting longitudinal nerves, a pair of ventro-lateral possessing multiple adhesive glands) and the diverse nerve cords along the trunk, and a terminal commissure. Paucitubulatina (possessing generally only two adhesive These features were also interpreted as ancestral condi- tubes) [24]. Muselliferidae, belonging to Paucitubulatina, tions of Gastrotricha in Kieneke and Schmidt-Rhaesa is the possible sister group to all remaining Paucitubula- (2015) [2, 12]. Yet only a single Paucitubulatina, Xenotri- tina according to morphological [22, 25] and molecular chula, was considered for this state reconstruction. More- [26, 27] studies. However, Paps and Riutorts [28] over, substantial variation exists, such as the presence of propose an alternative topology in which Xenotrichuli- an additional ventral nerve in Oregodasys cirratus Rothe dae is positioned as sister group of the remaining Pauci- & Schmidt-Rhaesa [38] and dorsal nerves in Xenodasys tubulatina, and Muselliferidae being the sister group to riedli (Schöpfer-Sterrer, 1969) [39, 40], or additional trunk Chaetonotidae. Kieneke et al. [29] find Proichthydiidae commissures in Dactylopodola and Oregodasys cirratus. as sister group to the remaining Paucitubulatina, with These studies highlight the unexplored diversity of gastro- Muselliferidae forming a clade together with Xenotrichuli- trich nervous systems, which may be especially relevant in dae sister group to other Paucitubulatina. These different the diverse group of Paucitubulatina, in which only one topologies overall suggest a key position of Muselliferidae study of the nervous system has been reported so far [13] within Gastrotricha, emphasizing the importance of this and given the
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